The Portland City Council unanimously confirmed Jon Jennings on Monday as the next city manager.

Jennings, 52, brings a diverse background to the city that includes time as president of the Maine Red Claws basketball franchise and as a senior adviser in the White House. He now co-owns a Red Mango frozen yogurt store in South Portland.

Mayor Michael Brennan said the position of city manager is “incredibly important” and Jenning’s broad experience will help the city.

“I think Jon is going to be an outstanding city manager,” Brennan said. “We need him at this particular time in this city’s history.”

Jennings’ only experience in municipal government is a two-year stint as South Portland’s assistant city manager. In Portland, he will run the day-to-day operations of the state’s largest city and oversee a staff of more than 1,400.

“He has a nontraditional background, but I think it’s the right background we need at this time,” Brennan said.

Councilors celebrated the appointment of Jennings, noting his background in professional sports, small business, development and, most recently, in South Portland. They also applauded his ability to be a strong manager who will lead the city.

“I think we got a gem here,” said Councilor Jill Duson.

Sixty-six people applied for the position in a nationwide search. The names of the other two finalists were never made public.

Jennings will start as city manager on July 13, under a three-year contract that will pay him a base salary of $148,064 a year. It will also require the Cape Elizabeth resident to move to Portland within a year.

“I am deeply honored beyond words to be standing before you with your vote of support,” said Jennings, who noted that 6½ years ago, he went before the council seeking a lease for the Red Claws at the Portland Expo.

“I am so passionate about Portland. I had the opportunity to put the Red Claws anywhere in New England, but I chose Portland,” he said. “It was the best decision I’ve ever made,” besides his wife and daughter.

Jennings will work with the City Council and the popularly elected mayor as both continue to define their respective roles and authority in the relatively new form of city government.

Councilor Kevin Donoghue said he was impressed by Jennings because of his “love of Portland that already exists and a really great attitude to help us address our issues as a group.”

Jennings has a master’s degree in public administration from Harvard University and served as a senior adviser for the White House’s Office of Cabinet Affairs under President Bill Clinton.

From 2005-07, Jennings oversaw Sen. John Kerry’s political operations in Massachusetts. He also served as an acting assistant U.S. attorney general.

Before taking the job in South Portland, he was president and co-owner of the Red Claws, an NBA Development League team, from 2007-12 and a general partner in the Thompson’s Point Development Co., which is undertaking an estimated $110 million redevelopment of nearly 30 acres of former industrial land along the Fore River.

Jennings led efforts to persuade Portland councilors to give the project a 30-year, $30 million tax break to facilitate the development, which calls for an arena/event center that would become the new home of the Red Claws, and up to 120 residential condominiums and a wide variety of other uses, including a circus school, office buildings, restaurants and an amphitheater.

Chris Thompson, who is leading the Thompson’s Point development, confirmed that Jennings relinquished a managing role in 2013 and recently divested himself of any financial interest in the project.

Jennings will take over during a period of significant transition at City Hall, with turnover occurring among top administrators and a flurry of real estate development that has caused both anxiety and optimism in the community.

Several high-profile decisions must be made about next year’s $221 million budget, including managing the possible closure of an emergency overflow homeless shelter, as well as reforms to the city’s General Assistance program.

Changes in the state budget and assistance policies have caused the city to consider closing the overflow shelter and cutting off General Assistance to asylum seekers starting July 1. Closing the shelter could put 75 people on the streets, and the General Assistance change could affect more than 900 immigrants who are seeking political asylum.